Bioinformatic Analysis Reveals Genome Size Reduction and the Emergence of Tyrosine Phosphorylation Site in the Movement Protein of New World Bipartite Begomoviruses

Abstract

Begomovirus (genus Begomovirus, family Geminiviridae) infection is devastating to a wide variety of agricultural crops including tomato, squash, and cassava. Thus, understanding the replication and adaptation of begomoviruses has important translational value in alleviating substantial economic loss, particularly in developing countries. The bipartite genome of begomoviruses prevalent in the New World and their counterparts in the Old World share a high degree of genome homology except for a partially overlapping reading frame encoding the pre-coat protein (PCP, or AV2). PCP contributes to the essential functions of intercellular movement and suppression of host RNA silencing, but it is only present in the Old World viruses. In this study, we analyzed a set of non-redundant bipartite begomovirus genomes originating from the Old World (N = 28) and the New World (N = 65). Our bioinformatic analysis suggests ∼120 nucleotides were deleted from PCP’s proximal promoter region that may have contributed to its loss in the New World viruses. Consequently, genomes of the New World viruses are smaller than the Old World counterparts, possibly compensating for the loss of the intercellular movement functions of PCP. Additionally, we detected substantial purifying selection on a portion of the New World DNA-B movement protein (MP, or BC1). Further analysis of the New World MP gene revealed the emergence of a putative tyrosine phosphorylation site, which likely explains the increased purifying selection in that region. These findings provide important information about the strategies adopted by bipartite begomoviruses in adapting to new environment and suggest future in planta experiments.

Vector-Enabled Metagenomic (VEM) Surveys Using Whiteflies (Aleyrodidae) Reveal Novel Begomovirus Species in the New and OldWorlds

“…Both genomic components, DNA-A and DNA-B, were recovered for eight of the genomes. These bipartite genomes exhibited general genomic features found in bipartite begomoviruses ( Supplemental Table S1 ), including a putative tyrosine phosphorylation site ([R/K]X 2,3 [D/E]X 2,3 Y) recently identified in the movement protein (MP) of NW bipartite begomoviruses [ 54 ]. The DNA-As of the remaining five genomes detected in the NW for which only one component was retrieved also exhibited characteristics suggesting that they represent one component of a bipartite begomovirus (as opposed to a monopartite virus).…”

“…The VEM approach allowed the recovery of both DNA-A and DNA-B components of several bipartite viruses in the NW. The genome size for all the components ( Supplemental Table S1 ) fell within average genome sizes for NW bipartite viruses, which on average have reduced genome sizes compared to their OW counterparts [ 54 ]. In addition to this size reduction, the MPs of the NW DNA-B components are under stronger purifying selective pressure than those of the OW viruses [ 54 ].…”

“…The genome size for all the components ( Supplemental Table S1 ) fell within average genome sizes for NW bipartite viruses, which on average have reduced genome sizes compared to their OW counterparts [ 54 ]. In addition to this size reduction, the MPs of the NW DNA-B components are under stronger purifying selective pressure than those of the OW viruses [ 54 ]. This stronger selection appears to maintain a putative tyrosine phosphorylation site found in the MP encoded by most NW DNA-B components [ 54 ], including all of the DNA-B components detected in this study ( Supplemental Table S1 ).…”

“…In addition to this size reduction, the MPs of the NW DNA-B components are under stronger purifying selective pressure than those of the OW viruses [ 54 ]. This stronger selection appears to maintain a putative tyrosine phosphorylation site found in the MP encoded by most NW DNA-B components [ 54 ], including all of the DNA-B components detected in this study ( Supplemental Table S1 ). However, NW DNA-A and DNA-B components seem to be under different evolutionary pressures, with the DNA-B exhibiting more overall genetic diversity than the DNA-A [ 74 ].…”

“…For several bipartite genomes detected in this study the DNA-B component was less similar to the DNA-B of previously characterized genomes than the DNA-A component, which exhibited higher identities to the DNA-A of known species ( Table 2 ). Therefore, although the genes encoded by DNA-B of NW viruses seem to be under more selective pressure compared to their OW counterparts [ 54 ], this component may still experience different evolutionary histories compared to its cognate DNA-A within the NW.…”